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. 1997 Jul;179(14):4545–4552. doi: 10.1128/jb.179.14.4545-4552.1997

The 75-kilodalton antigen of Bartonella bacilliformis is a structural homolog of the cell division protein FtsZ.

I Padmalayam 1, B Anderson 1, M Kron 1, T Kelly 1, B Baumstark 1
PMCID: PMC179290  PMID: 9226264

Abstract

A genomic library of Bartonella bacilliformis was constructed and screened with human anti-Bartonella serum from a patient with the chronic, verruga peruana phase of bartonellosis. An immunoreactive clone isolated from this library was found to code for a 591-amino-acid protein with a high degree of sequence similarity to the FtsZ family of proteins. The degree of amino acid identity between the B. bacilliformis protein (FtsZ[Bb]) and the other FtsZ proteins is especially pronounced over the N-terminal 321 amino acids (N-terminal domain) of the sequence, with values ranging from 45% identity for the homolog from Micrococcus luteus (FtsZ[Ml]) to 91% identity for the homolog from Rhizobium melliloti, (FtsZ[Rm1]). All of the functional domains required for FtsZ activity are conserved in FtsZ(Bb) and are located within the N-terminal domain of the protein. FtsZ(Bb) is approximately twice as large as most of the other FtsZ proteins previously reported, a property it shares with FtsZ(Rm1). Like the Rhizobium homolog, FtsZ(Bb) has a C-terminal region of approximately 256 amino acids that is absent in the other FtsZ proteins. Evidence is presented that implicates this region in the protein's antigenicity and suggests that, unlike most other FtsZ homologs, FtsZ(Bb) is at least partly exposed at the cell surface. PCR analysis revealed that an ftsZ gene similar in size to the B. bacilliformis gene is present in Bartonella henselae, a bacterium that is closely related to B. bacilliformis.

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Selected References

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  1. Anderson B., Goldsmith C., Johnson A., Padmalayam I., Baumstark B. Bacteriophage-like particle of Rochalimaea henselae. Mol Microbiol. 1994 Jul;13(1):67–73. doi: 10.1111/j.1365-2958.1994.tb00402.x. [DOI] [PubMed] [Google Scholar]
  2. Beall B., Lowe M., Lutkenhaus J. Cloning and characterization of Bacillus subtilis homologs of Escherichia coli cell division genes ftsZ and ftsA. J Bacteriol. 1988 Oct;170(10):4855–4864. doi: 10.1128/jb.170.10.4855-4864.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bi E. F., Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature. 1991 Nov 14;354(6349):161–164. doi: 10.1038/354161a0. [DOI] [PubMed] [Google Scholar]
  4. Brenner D. J., O'Connor S. P., Winkler H. H., Steigerwalt A. G. Proposals to unify the genera Bartonella and Rochalimaea, with descriptions of Bartonella quintana comb. nov., Bartonella vinsonii comb. nov., Bartonella henselae comb. nov., and Bartonella elizabethae comb. nov., and to remove the family Bartonellaceae from the order Rickettsiales. Int J Syst Bacteriol. 1993 Oct;43(4):777–786. doi: 10.1099/00207713-43-4-777. [DOI] [PubMed] [Google Scholar]
  5. Corton J. C., Ward J. E., Jr, Lutkenhaus J. Analysis of cell division gene ftsZ (sulB) from gram-negative and gram-positive bacteria. J Bacteriol. 1987 Jan;169(1):1–7. doi: 10.1128/jb.169.1.1-7.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dai K., Lutkenhaus J. ftsZ is an essential cell division gene in Escherichia coli. J Bacteriol. 1991 Jun;173(11):3500–3506. doi: 10.1128/jb.173.11.3500-3506.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dai K., Mukherjee A., Xu Y., Lutkenhaus J. Mutations in ftsZ that confer resistance to SulA affect the interaction of FtsZ with GTP. J Bacteriol. 1994 Jan;176(1):130–136. doi: 10.1128/jb.176.1.130-136.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Erickson H. P., Taylor D. W., Taylor K. A., Bramhill D. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):519–523. doi: 10.1073/pnas.93.1.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garcia F. U., Wojta J., Broadley K. N., Davidson J. M., Hoover R. L. Bartonella bacilliformis stimulates endothelial cells in vitro and is angiogenic in vivo. Am J Pathol. 1990 May;136(5):1125–1135. [PMC free article] [PubMed] [Google Scholar]
  10. Gray G. C., Johnson A. A., Thornton S. A., Smith W. A., Knobloch J., Kelley P. W., Obregon Escudero L., Arones Huayda M., Wignall F. S. An epidemic of Oroya fever in the Peruvian Andes. Am J Trop Med Hyg. 1990 Mar;42(3):215–221. doi: 10.4269/ajtmh.1990.42.215. [DOI] [PubMed] [Google Scholar]
  11. Holden P. R., Brookfield J. F., Jones P. Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster. Mol Gen Genet. 1993 Aug;240(2):213–220. doi: 10.1007/BF00277059. [DOI] [PubMed] [Google Scholar]
  12. Knobloch J. Analysis and preparation of Bartonella bacilliformis antigens. Am J Trop Med Hyg. 1988 Aug;39(2):173–178. doi: 10.4269/ajtmh.1988.39.173. [DOI] [PubMed] [Google Scholar]
  13. Kreier J. P., Ristic M. The biology of hemotrophic bacteria. Annu Rev Microbiol. 1981;35:325–338. doi: 10.1146/annurev.mi.35.100181.001545. [DOI] [PubMed] [Google Scholar]
  14. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  15. Lutkenhaus J. FtsZ ring in bacterial cytokinesis. Mol Microbiol. 1993 Aug;9(3):403–409. doi: 10.1111/j.1365-2958.1993.tb01701.x. [DOI] [PubMed] [Google Scholar]
  16. Margolin W., Corbo J. C., Long S. R. Cloning and characterization of a Rhizobium meliloti homolog of the Escherichia coli cell division gene ftsZ. J Bacteriol. 1991 Sep;173(18):5822–5830. doi: 10.1128/jb.173.18.5822-5830.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Margolin W., Long S. R. Rhizobium meliloti contains a novel second homolog of the cell division gene ftsZ. J Bacteriol. 1994 Apr;176(7):2033–2043. doi: 10.1128/jb.176.7.2033-2043.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McCormick J. R., Su E. P., Driks A., Losick R. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol Microbiol. 1994 Oct;14(2):243–254. doi: 10.1111/j.1365-2958.1994.tb01285.x. [DOI] [PubMed] [Google Scholar]
  19. Minnick M. F. Identification of outer membrane proteins of Bartonella bacilliformis. Infect Immun. 1994 Jun;62(6):2644–2648. doi: 10.1128/iai.62.6.2644-2648.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mitchell S. J., Minnick M. F. Characterization of a two-gene locus from Bartonella bacilliformis associated with the ability to invade human erythrocytes. Infect Immun. 1995 Apr;63(4):1552–1562. doi: 10.1128/iai.63.4.1552-1562.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mukherjee A., Lutkenhaus J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol. 1994 May;176(9):2754–2758. doi: 10.1128/jb.176.9.2754-2758.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. O'Connor S. P., Dorsch M., Steigerwalt A. G., Brenner D. J., Stackebrandt E. 16S rRNA sequences of Bartonella bacilliformis and cat scratch disease bacillus reveal phylogenetic relationships with the alpha-2 subgroup of the class Proteobacteria. J Clin Microbiol. 1991 Oct;29(10):2144–2150. doi: 10.1128/jcm.29.10.2144-2150.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. RayChaudhuri D., Park J. T. A point mutation converts Escherichia coli FtsZ septation GTPase to an ATPase. J Biol Chem. 1994 Sep 16;269(37):22941–22944. [PubMed] [Google Scholar]
  24. RayChaudhuri D., Park J. T. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature. 1992 Sep 17;359(6392):251–254. doi: 10.1038/359251a0. [DOI] [PubMed] [Google Scholar]
  25. Regnery R. L., Anderson B. E., Clarridge J. E., 3rd, Rodriguez-Barradas M. C., Jones D. C., Carr J. H. Characterization of a novel Rochalimaea species, R. henselae sp. nov., isolated from blood of a febrile, human immunodeficiency virus-positive patient. J Clin Microbiol. 1992 Feb;30(2):265–274. doi: 10.1128/jcm.30.2.265-274.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Relman D. A., Loutit J. S., Schmidt T. M., Falkow S., Tompkins L. S. The agent of bacillary angiomatosis. An approach to the identification of uncultured pathogens. N Engl J Med. 1990 Dec 6;323(23):1573–1580. doi: 10.1056/NEJM199012063232301. [DOI] [PubMed] [Google Scholar]
  27. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tashiro K., Hagiya M., Nishizawa T., Seki T., Shimonishi M., Shimizu S., Nakamura T. Deduced primary structure of rat hepatocyte growth factor and expression of the mRNA in rat tissues. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3200–3204. doi: 10.1073/pnas.87.8.3200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Voskuil J. L., Westerbeek C. A., Wu C., Kolk A. H., Nanninga N. Epitope mapping of Escherichia coli cell division protein FtsZ with monoclonal antibodies. J Bacteriol. 1994 Apr;176(7):1886–1893. doi: 10.1128/jb.176.7.1886-1893.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. de Boer P., Crossley R., Rothfield L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature. 1992 Sep 17;359(6392):254–256. doi: 10.1038/359254a0. [DOI] [PubMed] [Google Scholar]

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